The dispersion of the water H-1 longitudinal relaxation rate in the frequency range 2-100 MHz has been measured in aqueous solutions of bovine pancreatic trypsin inhibitor (BPTI) and a mutant protein (G36S) lacking one of the four internal water molecules. The H-1 relaxation dispersion has also been measured for BPTI in a series of H2O/D2O mixtures. The quantitative analysis of these data resolve the major controversies in the interpretation of water H-1 relaxation data from protein solutions and has implications for medical magnetic resonance imaging. Three principal conclusions are drawn. First, as previously found for the water H-2 and O-17 dispersions, the BPTI G36S difference H-1 dispersion can be quantitatively accounted for by a single, fully ordered, internal water molecule (W122). The intrinsic relaxation rate of these water protons is ca. 70% intramolecular, with the intramolecular dipole coupling constant as in ice, and ca. 30% intermolecular, with significant dipole couplings to many BPTI protons. Second, exchanging protons in the protein make a substantial contribution to the observed water H-1 relaxation rate. This contribution should be dominant even at neutral pH for most proteins. Third, the effect of intermolecular dipole couplings with protein protons is additive, and cross-relaxation effects are negligible. A theoretical analysis of dipole relaxation in a multispin system undergoing chemical exchange with an abundant bulk phase shows that this conclusion holds generally within the regime of motional narrowing theory.